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Adherence to Standard of Care in the Diagnosis and Treatment of Suspected Bacterial Meningitis David Chia, Youness Yavari, Eugeny Kirsanov, Steven I. Aronin and Majid Sadigh American Journal of Medical Quality published online 1 August 2014 DOI: 10.1177/1062860614545778 The online version of this article can be found at: http://ajm.sagepub.com/content/early/2014/07/31/1062860614545778
Published by: http://www.sagepublications.com
On behalf of: American College of Medical Quality
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545778
research-article2014
AJMXXX10.1177/1062860614545778American Journal of Medical QualityChia et al
Article
Adherence to Standard of Care in the Diagnosis and Treatment of Suspected Bacterial Meningitis
American Journal of Medical Quality 1–4 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1062860614545778 ajmq.sagepub.com
David Chia, MD, MS1, Youness Yavari, MD2, Eugeny Kirsanov, MD3, Steven I. Aronin, MD1, and Majid Sadigh, MD2
Abstract Acute bacterial meningitis (ABM) is a rare but deadly neurological emergency. Accordingly, Infectious Diseases Society of America (IDSA) guidelines summarize current evidence into a straightforward algorithm for its management. The goal of this study is to evaluate the overall compliance with these guidelines in patients with suspected ABM. A retrospective cross-sectional study was conducted of adult patients who underwent lumbar puncture for suspected ABM to ascertain local adherence patterns to IDSA guidelines for bacterial meningitis. Primary outcomes included appropriate utilization of neuroimaging, blood cultures, antibiotics, corticosteroids, and lumbar puncture. In all, 160 patients were included in the study. Overall IDSA compliance was only 0.6%. Neuroimaging and blood cultures were appropriately utilized in 54.3% and 47.5% of patients, respectively. Steroids and antibiotics were appropriately administered in only 7.5% and 5.6% of patients, respectively. Adherence to IDSA guidelines is poor. Antibiotic choice is often incorrect, corticosteroids are rarely administered, and there is an overutilization of neuroimaging. Keywords bacterial meningitis, guidelines, adherence, standard of care In the United States, acute bacterial meningitis (ABM) remains a rare but deadly neurological emergency. The annual incidence of ABM is estimated to be only 3 per 100 000; however, both morbidity and mortality remain high despite antibiotic therapy.1 One contemporary study of individuals at least 16 years of age demonstrated a case fatality rate of 27% with persistent neurologic deficits present in 9% of survivors.2 As a result, it is important that patients with suspected ABM are managed efficiently such that empiric antibiotics and corticosteroids are administered without delay and simultaneous with diagnostic testing. Accordingly, Infectious Diseases Society of America (IDSA) guidelines published in 2004 summarize current evidence and expert opinion into a straightforward algorithm for the management of ABM.3 The goal of this study is to evaluate the overall compliance with the IDSA guidelines in the diagnostic evaluation and treatment of patients with suspected ABM.
Methods A one-year retrospective cross-sectional study was conducted at 3 community teaching hospitals in Connecticut
(Waterbury Hospital, Waterbury, CT; St. Mary’s Hospital, Waterbury, CT; and Danbury Hospital, Danbury, CT) from September 2010 through August 2011. Patients met criteria for inclusion into the study if they were ≥18 years of age, had a lumbar puncture (LP) performed within 24 hours of hospital presentation, and the indication for LP was documented in the medical record as being to evaluate for suspected ABM. Data extraction from the medical record was performed utilizing a standardized form. Extracted data included information on demographics, clinical presentation, diagnostic testing, and treatment. Primary outcomes of the study included timing and appropriate utilization of neuroimaging, LP, blood cultures, corticosteroids, and antibiotics.
1
Waterbury Hospital, Waterbury, CT Danbury Hospital, Danbury, CT 3 St Mary’s Hospital, Waterbury, CT 2
Corresponding Author: David Chia, MD, MS, Yale Primary Care Residency Program, Waterbury Hospital, 64 Robbins Street, Waterbury, CT 06708. Email: [email protected]
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American Journal of Medical Quality
Table 1. Clinical Presentation of Patients With Suspected Bacterial Meningitis. Clinical Symptoms Headache Subjective fever Neck stiffness Altered mental status
Clinical Signs 88% (133/151) 60% (93/156) 42% (49/116) 25% (39/158)
Tachycardia (HR ≥ 90) Objective fever (T ≥ 38°C) Altered mental status Nuchal rigidity
64% (103/160) 32% (51/160) 20% (31/152) 9% (13/146)
Abbreviations: HR, heart rate; T, temperature.
Table 2. IDSA Guideline Adherence.
Head CT scan Head CT indicated Head CT performed Blood culture Blood culture obtained Blood culture obtained before antibiotics Steroid Administered Administered with/before antibiotics Correct dose Antibiotics Antibiotics administered Antibiotics administered before head CT Correct antibiotic choice/dose Overall IDSA guideline
Percentage
Adherence to IDSA Guidelines
31.9% (51/160) 73.7% (118/160)
54.3% (87/160)
53.7% (86/160) 85.5% (59/69)
47.5% (76/160)
9.3% (15/160) 90% (9/10) 80% (8/10)
7.5% (12/160)
50% (80/160) 41.3% (24/58) 18.7% (15/80)
5.6% (9/160)
0.6 (1/160)
Abbreviations: CT, computed tomography; IDSA, Infectious Diseases Society of America.
Adherence to neuroimaging was determined by whether the patient had an appropriate indication for head computed tomography (CT; immunocompromised host, central nervous system disease, new onset seizure within 1 week, and new focal neurologic deficit) and if the head CT was obtained before LP was performed. Adherence to blood cultures was determined by whether blood cultures were drawn and whether it was performed prior to antibiotic administration. Adherence to corticosteroids was determined by whether they were administered and, if they were administered, whether they were given before or concomitantly with antibiotics and at the correct dose (dexamethasone 0.15 mg/kg). Adherence to antibiotics was determined by whether corticosteroids were administered; if they were administered, whether the appropriate regimen and dose were prescribed as defined by the IDSA guidelines; and if they were given before head CT (if a head CT was obtained) or after LP (if a head CT was not obtained).
Overall adherence was determined by complete adherence with respect to neuroimaging, blood cultures, corticosteroids, and antibiotics.
Results A total of 160 patients met the inclusion criteria for the study. The mean age of the study population was 43 years (standard deviation [SD] = 18.1), and 55% of the patients were female. In terms of comorbid conditions, 9% of patients were immunocompromised, 5% of whom were HIV positive, 5% had a known malignancy, 25% were obese, 9% were diabetic, 6% had a history of alcohol abuse, and 2% had a history of injectable drug use. The most common clinical presentation was headache and subjective fever. The most common objective features on clinical examination were tachycardia and fever (Table 1). Neuroimaging was appropriately utilized in 54.3% of patients (Table 2). CT of the head was indicated in almost one third of patients, but it was performed in almost three quarters of patients. In approximately 9%
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Chia et al of the cases CT was performed after LP. In one of these cases, the patient did have a contraindication against immediate LP and should have had neuroimaging prior to the procedure given focal neurologic findings on examination. However, no complications occurred despite this. As shown in Table 2, blood cultures were appropriately obtained in almost 48% of patients. Blood cultures were positive in 11.6% of patients; Streptococcus pneumoniae was responsible for 60%, while Group B Streptococcus, Staphylococcus aureus, Escherichia coli, and Listeria accounted for the remaining 40%. Mean time to LP was 297.3 minutes (SD = 214.1) in patients receiving neuroimaging and 349.6 minutes (SD = 288.8) in those not receiving neuroimaging. Cerebrospinal fluid studies were positive in 3.1%. The causative organisms in these cases included Streptococcus pneumoniae, Group B Streptococcus, and herpes simplex virus. Table 2 shows that corticosteroids and antibiotics were seldom utilized appropriately in terms of choice, dose, and timing. Of the 160 total patients, only 50% received empiric antibiotics and only 9% received corticosteroids. Major failures in treatment adherence included failure to administer empiric antibiotics (50%), incorrect antibiotic choice (71%), incorrect antibiotic dose (46%), and failure to receive antibiotics prior to neuroimaging (58.7%). Based on the utilization of neuroimaging, adherence to blood culture, antibiotics, and corticosteroids, the overall IDSA compliance was determined to be only 0.6% (1/160).
Discussion This study found that adherence to IDSA guidelines in the diagnosis and treatment of suspected ABM in the studied hospitals was poor. Antibiotic choice, dose, and timing were often incorrect and steroids were rarely administered. Blood cultures were not commonly obtained. Moreover, there was overutilization of neuroimaging, prompting delays in treatment and increased health care costs. In their totality, these findings demonstrate a failure to successfully implement evidence-based guidelines and may have negatively affected clinical outcomes. These findings are supported by the results of other similar studies. Georges et al reported 65% compliance with IDSA guidelines for patients with bacterial meningitis hospitalized in an intensive care unit in France.4 Noncompliance in this study was mostly related to vancomycin nondelivery or incorrect dosing and was associated
with increased mortality. Stockdale et al evaluated 39 patients with ABM in a British teaching hospital and found that immediate LP for those with no contraindications was carried out in only 17% of cases and that only 65% of patients received antibiotics within 3 hours of arrival.5 Although both the aforementioned studies evaluated adherence to standard of care for patients with ABM, the present study has notable methodological differences. First, it took place in the emergency department at 3 community-based teaching hospitals in the United States. Second, it included all patients with suspected ABM, not just those with proven bacterial etiology. Consequently, the research team believes that the approach used in the present study yielded data that more accurately reflect real-life clinical practice and guideline compliance than the previous studies. Third, the present study required clinicians to adhere to all steps within the IDSA guideline in order to be considered compliant. The research team feels that this methodological requirement was essential in order to ascertain whether patients with presumed ABM, a condition with high mortality if left untreated, are receiving the diagnostic and therapeutic interventions needed to optimize their chance of survival. The research team suspects that the primary reason for guideline underutilization may be related to the low frequency of ABM in the United States. Put simply, clinicians may be more likely to use guidelines for disease states they see commonly than for diseases they see infrequently. There are several other potential reasons why this study found poor adherence with the IDSA guidelines, including clinician lack of knowledge about how to manage patients with ABM, clinician lack of awareness that the IDSA guideline exists, and clinician belief that certain clinical features of a given patient make an alternate diagnosis more likely than ABM. Limitations of this study include its retrospective study design and its reliance on chart documentation and completeness. The research team hopes that these findings will result in enhanced education for those clinicians and departments likely to encounter patients with signs and symptoms of ABM. Such educational sessions should focus on the fact that there is very little clinical distinction between patients presenting with bacterial and nonbacterial meningitis and that all patients with signs and symptoms of meningitis should be approached in a similar fashion so that the rare individual with ABM will have the best chance of survival. Furthermore, all emergency departments should make the IDSA practice guideline for the management of ABM readily available to its clinicians.
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American Journal of Medical Quality
In turn, all clinicians should familiarize themselves with the contents of this protocol. In addition, future research is needed to optimize the management of patients with suspected and confirmed ABM. Potential areas of research include studying why clinicians fail to adhere to published guidelines, identification of barriers to guideline adherence, and the impact of novel strategies to improve guideline compliance. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
References 1. Attia J, Hatala R, Cook DJ, Wong JG. Does this adult patient have acute meningitis? JAMA. 1999;282:175-181. 2. Aronin SI, Peduzzi P, Quagliarello VJ. Community-acquired bacterial meningitis: risk stratification for adverse clinical outcome and effect of antibiotic timing. Ann Intern Med. 1998;129:862-869. 3. Tunkel AR, Hartman BJ, Kaplan SL, et al. Practice guidelines for the management of bacterial meningitis. Clin Infect Dis. 2004;39:1267-1284. 4. Georges H, Chiche A, Alfandari S, Devos P, Boussekey N, Leroy O. Adult community-acquired bacterial meningitis requiring ICU admission: epidemiological data, prognosis factors and adherence to IDSA guidelines. Eur J Clin Microbiol Infect Dis. 2009;28:1317-1325. 5. Stockdale AJ, Weekes MP, Aliyu SH. An audit of acute bacterial meningitis in a large teaching hospital 2005-10. QJM. 2011;104:1055-1063.
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Adherence to Standard of Care in the Diagnosis and Treatment of Suspected Bacterial Meningitis David Chia, Youness Yavari, Eugeny Kirsanov, Steven I. Aronin and Majid Sadigh American Journal of Medical Quality published online 1 August 2014 DOI: 10.1177/1062860614545778 The online version of this article can be found at: http://ajm.sagepub.com/content/early/2014/07/31/1062860614545778
Published by: http://www.sagepublications.com
On behalf of: American College of Medical Quality
Additional services and information for American Journal of Medical Quality can be found at: Email Alerts: http://ajm.sagepub.com/cgi/alerts Subscriptions: http://ajm.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> OnlineFirst Version of Record - Aug 1, 2014 What is This?
Downloaded from ajm.sagepub.com at GEORGIAN COURT UNIV on October 20, 2014
545778
research-article2014
AJMXXX10.1177/1062860614545778American Journal of Medical QualityChia et al
Article
Adherence to Standard of Care in the Diagnosis and Treatment of Suspected Bacterial Meningitis
American Journal of Medical Quality 1–4 © The Author(s) 2014 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/1062860614545778 ajmq.sagepub.com
David Chia, MD, MS1, Youness Yavari, MD2, Eugeny Kirsanov, MD3, Steven I. Aronin, MD1, and Majid Sadigh, MD2
Abstract Acute bacterial meningitis (ABM) is a rare but deadly neurological emergency. Accordingly, Infectious Diseases Society of America (IDSA) guidelines summarize current evidence into a straightforward algorithm for its management. The goal of this study is to evaluate the overall compliance with these guidelines in patients with suspected ABM. A retrospective cross-sectional study was conducted of adult patients who underwent lumbar puncture for suspected ABM to ascertain local adherence patterns to IDSA guidelines for bacterial meningitis. Primary outcomes included appropriate utilization of neuroimaging, blood cultures, antibiotics, corticosteroids, and lumbar puncture. In all, 160 patients were included in the study. Overall IDSA compliance was only 0.6%. Neuroimaging and blood cultures were appropriately utilized in 54.3% and 47.5% of patients, respectively. Steroids and antibiotics were appropriately administered in only 7.5% and 5.6% of patients, respectively. Adherence to IDSA guidelines is poor. Antibiotic choice is often incorrect, corticosteroids are rarely administered, and there is an overutilization of neuroimaging. Keywords bacterial meningitis, guidelines, adherence, standard of care In the United States, acute bacterial meningitis (ABM) remains a rare but deadly neurological emergency. The annual incidence of ABM is estimated to be only 3 per 100 000; however, both morbidity and mortality remain high despite antibiotic therapy.1 One contemporary study of individuals at least 16 years of age demonstrated a case fatality rate of 27% with persistent neurologic deficits present in 9% of survivors.2 As a result, it is important that patients with suspected ABM are managed efficiently such that empiric antibiotics and corticosteroids are administered without delay and simultaneous with diagnostic testing. Accordingly, Infectious Diseases Society of America (IDSA) guidelines published in 2004 summarize current evidence and expert opinion into a straightforward algorithm for the management of ABM.3 The goal of this study is to evaluate the overall compliance with the IDSA guidelines in the diagnostic evaluation and treatment of patients with suspected ABM.
Methods A one-year retrospective cross-sectional study was conducted at 3 community teaching hospitals in Connecticut
(Waterbury Hospital, Waterbury, CT; St. Mary’s Hospital, Waterbury, CT; and Danbury Hospital, Danbury, CT) from September 2010 through August 2011. Patients met criteria for inclusion into the study if they were ≥18 years of age, had a lumbar puncture (LP) performed within 24 hours of hospital presentation, and the indication for LP was documented in the medical record as being to evaluate for suspected ABM. Data extraction from the medical record was performed utilizing a standardized form. Extracted data included information on demographics, clinical presentation, diagnostic testing, and treatment. Primary outcomes of the study included timing and appropriate utilization of neuroimaging, LP, blood cultures, corticosteroids, and antibiotics.
1
Waterbury Hospital, Waterbury, CT Danbury Hospital, Danbury, CT 3 St Mary’s Hospital, Waterbury, CT 2
Corresponding Author: David Chia, MD, MS, Yale Primary Care Residency Program, Waterbury Hospital, 64 Robbins Street, Waterbury, CT 06708. Email: [email protected]
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American Journal of Medical Quality
Table 1. Clinical Presentation of Patients With Suspected Bacterial Meningitis. Clinical Symptoms Headache Subjective fever Neck stiffness Altered mental status
Clinical Signs 88% (133/151) 60% (93/156) 42% (49/116) 25% (39/158)
Tachycardia (HR ≥ 90) Objective fever (T ≥ 38°C) Altered mental status Nuchal rigidity
64% (103/160) 32% (51/160) 20% (31/152) 9% (13/146)
Abbreviations: HR, heart rate; T, temperature.
Table 2. IDSA Guideline Adherence.
Head CT scan Head CT indicated Head CT performed Blood culture Blood culture obtained Blood culture obtained before antibiotics Steroid Administered Administered with/before antibiotics Correct dose Antibiotics Antibiotics administered Antibiotics administered before head CT Correct antibiotic choice/dose Overall IDSA guideline
Percentage
Adherence to IDSA Guidelines
31.9% (51/160) 73.7% (118/160)
54.3% (87/160)
53.7% (86/160) 85.5% (59/69)
47.5% (76/160)
9.3% (15/160) 90% (9/10) 80% (8/10)
7.5% (12/160)
50% (80/160) 41.3% (24/58) 18.7% (15/80)
5.6% (9/160)
0.6 (1/160)
Abbreviations: CT, computed tomography; IDSA, Infectious Diseases Society of America.
Adherence to neuroimaging was determined by whether the patient had an appropriate indication for head computed tomography (CT; immunocompromised host, central nervous system disease, new onset seizure within 1 week, and new focal neurologic deficit) and if the head CT was obtained before LP was performed. Adherence to blood cultures was determined by whether blood cultures were drawn and whether it was performed prior to antibiotic administration. Adherence to corticosteroids was determined by whether they were administered and, if they were administered, whether they were given before or concomitantly with antibiotics and at the correct dose (dexamethasone 0.15 mg/kg). Adherence to antibiotics was determined by whether corticosteroids were administered; if they were administered, whether the appropriate regimen and dose were prescribed as defined by the IDSA guidelines; and if they were given before head CT (if a head CT was obtained) or after LP (if a head CT was not obtained).
Overall adherence was determined by complete adherence with respect to neuroimaging, blood cultures, corticosteroids, and antibiotics.
Results A total of 160 patients met the inclusion criteria for the study. The mean age of the study population was 43 years (standard deviation [SD] = 18.1), and 55% of the patients were female. In terms of comorbid conditions, 9% of patients were immunocompromised, 5% of whom were HIV positive, 5% had a known malignancy, 25% were obese, 9% were diabetic, 6% had a history of alcohol abuse, and 2% had a history of injectable drug use. The most common clinical presentation was headache and subjective fever. The most common objective features on clinical examination were tachycardia and fever (Table 1). Neuroimaging was appropriately utilized in 54.3% of patients (Table 2). CT of the head was indicated in almost one third of patients, but it was performed in almost three quarters of patients. In approximately 9%
Downloaded from ajm.sagepub.com at GEORGIAN COURT UNIV on October 20, 2014
3
Chia et al of the cases CT was performed after LP. In one of these cases, the patient did have a contraindication against immediate LP and should have had neuroimaging prior to the procedure given focal neurologic findings on examination. However, no complications occurred despite this. As shown in Table 2, blood cultures were appropriately obtained in almost 48% of patients. Blood cultures were positive in 11.6% of patients; Streptococcus pneumoniae was responsible for 60%, while Group B Streptococcus, Staphylococcus aureus, Escherichia coli, and Listeria accounted for the remaining 40%. Mean time to LP was 297.3 minutes (SD = 214.1) in patients receiving neuroimaging and 349.6 minutes (SD = 288.8) in those not receiving neuroimaging. Cerebrospinal fluid studies were positive in 3.1%. The causative organisms in these cases included Streptococcus pneumoniae, Group B Streptococcus, and herpes simplex virus. Table 2 shows that corticosteroids and antibiotics were seldom utilized appropriately in terms of choice, dose, and timing. Of the 160 total patients, only 50% received empiric antibiotics and only 9% received corticosteroids. Major failures in treatment adherence included failure to administer empiric antibiotics (50%), incorrect antibiotic choice (71%), incorrect antibiotic dose (46%), and failure to receive antibiotics prior to neuroimaging (58.7%). Based on the utilization of neuroimaging, adherence to blood culture, antibiotics, and corticosteroids, the overall IDSA compliance was determined to be only 0.6% (1/160).
Discussion This study found that adherence to IDSA guidelines in the diagnosis and treatment of suspected ABM in the studied hospitals was poor. Antibiotic choice, dose, and timing were often incorrect and steroids were rarely administered. Blood cultures were not commonly obtained. Moreover, there was overutilization of neuroimaging, prompting delays in treatment and increased health care costs. In their totality, these findings demonstrate a failure to successfully implement evidence-based guidelines and may have negatively affected clinical outcomes. These findings are supported by the results of other similar studies. Georges et al reported 65% compliance with IDSA guidelines for patients with bacterial meningitis hospitalized in an intensive care unit in France.4 Noncompliance in this study was mostly related to vancomycin nondelivery or incorrect dosing and was associated
with increased mortality. Stockdale et al evaluated 39 patients with ABM in a British teaching hospital and found that immediate LP for those with no contraindications was carried out in only 17% of cases and that only 65% of patients received antibiotics within 3 hours of arrival.5 Although both the aforementioned studies evaluated adherence to standard of care for patients with ABM, the present study has notable methodological differences. First, it took place in the emergency department at 3 community-based teaching hospitals in the United States. Second, it included all patients with suspected ABM, not just those with proven bacterial etiology. Consequently, the research team believes that the approach used in the present study yielded data that more accurately reflect real-life clinical practice and guideline compliance than the previous studies. Third, the present study required clinicians to adhere to all steps within the IDSA guideline in order to be considered compliant. The research team feels that this methodological requirement was essential in order to ascertain whether patients with presumed ABM, a condition with high mortality if left untreated, are receiving the diagnostic and therapeutic interventions needed to optimize their chance of survival. The research team suspects that the primary reason for guideline underutilization may be related to the low frequency of ABM in the United States. Put simply, clinicians may be more likely to use guidelines for disease states they see commonly than for diseases they see infrequently. There are several other potential reasons why this study found poor adherence with the IDSA guidelines, including clinician lack of knowledge about how to manage patients with ABM, clinician lack of awareness that the IDSA guideline exists, and clinician belief that certain clinical features of a given patient make an alternate diagnosis more likely than ABM. Limitations of this study include its retrospective study design and its reliance on chart documentation and completeness. The research team hopes that these findings will result in enhanced education for those clinicians and departments likely to encounter patients with signs and symptoms of ABM. Such educational sessions should focus on the fact that there is very little clinical distinction between patients presenting with bacterial and nonbacterial meningitis and that all patients with signs and symptoms of meningitis should be approached in a similar fashion so that the rare individual with ABM will have the best chance of survival. Furthermore, all emergency departments should make the IDSA practice guideline for the management of ABM readily available to its clinicians.
Downloaded from ajm.sagepub.com at GEORGIAN COURT UNIV on October 20, 2014
4
American Journal of Medical Quality
In turn, all clinicians should familiarize themselves with the contents of this protocol. In addition, future research is needed to optimize the management of patients with suspected and confirmed ABM. Potential areas of research include studying why clinicians fail to adhere to published guidelines, identification of barriers to guideline adherence, and the impact of novel strategies to improve guideline compliance. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
References 1. Attia J, Hatala R, Cook DJ, Wong JG. Does this adult patient have acute meningitis? JAMA. 1999;282:175-181. 2. Aronin SI, Peduzzi P, Quagliarello VJ. Community-acquired bacterial meningitis: risk stratification for adverse clinical outcome and effect of antibiotic timing. Ann Intern Med. 1998;129:862-869. 3. Tunkel AR, Hartman BJ, Kaplan SL, et al. Practice guidelines for the management of bacterial meningitis. Clin Infect Dis. 2004;39:1267-1284. 4. Georges H, Chiche A, Alfandari S, Devos P, Boussekey N, Leroy O. Adult community-acquired bacterial meningitis requiring ICU admission: epidemiological data, prognosis factors and adherence to IDSA guidelines. Eur J Clin Microbiol Infect Dis. 2009;28:1317-1325. 5. Stockdale AJ, Weekes MP, Aliyu SH. An audit of acute bacterial meningitis in a large teaching hospital 2005-10. QJM. 2011;104:1055-1063.
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